Identification and Dynamics of Two Classes of Aurora-Like Kinases in Arabidopsis and Other Plants

Abstract

Aurora-like kinases play key roles in chromosome segregation and cytokinesis in yeast, plant, and animal systems. Here, we characterize three Arabidopsis thaliana protein kinases, designated AtAurora1, AtAurora2, and AtAurora3, which share high amino acid identities with the Ser/Thr kinase domain of yeast Ipl1 and animal Auroras. Structure and expression of AtAurora1 and AtAurora2 suggest that these genes arose by a recent gene duplication, whereas the diversification of plant α and β Aurora kinases predates the origin of land plants. The transcripts and proteins of all three kinases are most abundant in tissues containing dividing cells. Intracellular localization of green fluorescent protein–tagged AtAuroras revealed an AtAurora-type specific association mainly with dynamic mitotic structures, such as microtubule spindles and centromeres, and with the emerging cell plate of dividing tobacco (Nicotiana tabacum) BY-2 cells. Immunolabeling using AtAurora antibodies yielded specific signals at the centromeres that are coincident with histone H3 that is phosphorylated at Ser position10 during mitosis. An in vitro kinase assay demonstrated that AtAurora1 preferentially phosphorylates histone H3 at Ser 10 but not at Ser 28 or Thr 3, 11, and 32. The phylogenetic analysis of available Aurora sequences from different eukaryotic origins suggests that, although a plant Aurora gene has been duplicated early in the evolution of plants, the paralogs nevertheless maintained a role in cell cycle–related signal transduction pathways.

Impact of nucleosome dynamics and histone modifications on cell proliferation during Arabidopsis development

“…Multiple kinases have been identified in mammalian cells that show H3 phosphorylation activity (Ito, 2007). The Arabidopsis homologs of AURORA (AUR1-3) kinases are highly expressed in mitosis and can efficiently use H3 as a substrate, consistent with a role at this stage (Demidov et al, 2005;Kawabe et al, 2005;Kurihara et al, 2006). The TOUSLED (TSL) kinase is expressed at a constant rate during the cell cycle but its activity peaks between late G2/M and the next G1 phase and H3 is also a known substrate (Figure 1) (Ehsan et al, 2004), although conflicting reports exist regarding the role of TSL on H3 phosphorylation .…”

Mitosis-specific kinesins in Arabidopsis

“…In addition to control by CDK-type kinases, Aurora kinases have also been shown to play important roles in the regulation of the subcellular localization of Kinesin-6 kinesins through phosphorylation. Aurora kinases are present in plants and localize to the spindle and cell plate [19]. Because Kinesin-6 kinesins are absent in Arabidopsis, it remains to be seen whether Aurora kinases have a role in kinesin regulation.…”

Mechanisms of plant spindle formation

“…This mechanism is entirely consistent with the available limited literature on plants. Aurora kinases are present in plants and bind to kinetochores (Demidov et al 2005), and homologs of Ndc80 and Mis12 have been identified in maize and localize outside the inner kinetochores (Du and Dawe 2007;Li and Dawe 2009). Other components of the Ndc80 complex can also be detected in plants by sequence similarity (Meraldi et al 2006) but have not yet been shown to be kinetochore-localized or to interact directly with Ndc80.…”